The Comparative Method in Evolutionary Biology

Oxford Series in Ecology and Evolution, vol. 1
Oxford University Press, 1991

On the Uses of Knowing Where Birds and Bees Come From

Comparative studies in biology are older than acceptance of evolution, but that
acceptance makes them both more important, and harder to do right. The
importance comes from questions about adaptation and causation. We would very
much like to know what traits of organisms are adaptations to what
circumstances --- even to know which adaptations opened the way for which other
adaptations. They get harder because, if Darwin is at all right, we should
expect species descended from a common ancestor to resemble each other simply
because they are so descended, and not necessarily because their
common traits have common adaptive functions.

A (reasonably) concrete example may make the point clear. Dolphins, marlins
and the sadly extinct marine reptiles called icthyosaurs all have similar
profiles, and it's reasonable to think that they do so because that shape is
an efficient one for moving a large animal through water fast enough to catch
and eat much smaller animals. To test this idea comparatively, we need to look
for four sorts of marine animals: those with a streamlined,
dolphin-like shape who are large and pursue small, fast fish; those with the
shape which do not fill that niche; those which do fill that niche which do not
have that shape; and those which neither have that shape nor fill that niche.
The naive approach is to total up all the species under each heading we can
find, fill out what the statisticians call a "contingency table," and then
apply one of the standard statistical tests to see whether or not there is a
significant correlation between having a dolphin-like shape and filling a
dolphin-like niche. The problem is that those tests all assume that the
data-points are independent of each other. In this case, however, related
species are not independent samples: all dolphin species resemble each
other not just because they occupy similar niches, but because they share a
common ancestry. If the ancestral proto-dolphin had both the shape and the
niche, then we expect most of its descendants to have both, and so the
association between the characters would have to do with descent and not
natural selection. In that case, we shouldn't count all the modern
dolphins in our contingency table --- but how many dolphins should we
count? Just one, for the common ancestor? More than one, to reflect the fact
that the traits haven't become detached in subsequent evolution? If so, how
many more than one? And what do we do about, e.g., the common ancestor of
whales and dolphins?

The problem to solve, then, is to find some way of dividing up our
information about contemporary species into statistically independent chunks,
and it's clear that doing this right will need information about phylogeny
(which species are related to which others, when they diverged, etc.),
ancestral characters, and the dynamics of evolution. We need phylogenies to
know which species are related, so that we don't count them as independent; we
need to know ancestral traits so that we can figure out what has evolved when;
and we need to know evolutionary dynamics to get an idea of how often we should
expect "chance" (i.e. non-adaptive) associations. (Knowing phylogenies and
ancestral traits also lets us test ideas about the direction of
evolution --- do marine animals first become predators and then get
dolphin-shaped, or vice versa?) It's important to realize that these models of
random evolution are just null hypotheses --- which does not mean that we
expect most evolution to be non-adaptive!

Statistical methods which take proper account of phylogeny and evolutionary
dynamics have only really been developed within the last twenty-odd years. In
part this is because of the rising availability of really reliable phylogenies,
especially from comparing the DNA and proteins of different species, and using
the known rates at which they accumulate random errors --- "molecular
clocks." (The number of such publications in molecular phylogeny is currently
doubling every two years.) Harvey and Pagel are two of the leading figures in
applying the new data and the new models to comparative studies, and this book
is their introduction to the newer methods.

They begin with a chapter on why comparative studies are desirable, and why
they are hard. This is followed with a chapter which seeks to convince
comparativists that they ignore phylogeny at their peril. That done, one wants
to know how to construct a phylogeny, and more importantly how to figure out
the characters of ancestral species from those of existing ones.
Unfortunately, proper phylogenetic methods are the subject of some of the most vehement and technical controversies in modern
biology. Harvey and Pagel's advice on this point is basically to leave the
controversy to the specialists, but to go with molecular data when you can get
it. (They also describe the dangers of trying to use standard taxonomies as
substitute phylogenies.)

Chapter four describes the "comparative analysis of discrete data":
qualitative characters which are described as taking one of a few different
states. (Our initial example, of marine-animal shape and niche, would be an
instance of this.) The key idea here is that, while the characters of related
species are not independent, the changes in characters along separate
lineages are. After a quick survey of previous methods which use this idea,
Harvey and Pagel present one of their own, which takes into account the fact
that more evolutionary change should be expected over long periods of time than
over short ones, and estimates the rates at which traits are changing in the
species of interest. Chapter five goes through a similar analysis for
continuous traits, advocating the method of "independent comparisons" (using
the differences between pairs of species as independent variables),
and elaborating null models based on Brownian motion and randomizations of the
original data. (We could apply these techniques to our marine example if we
made use of some of the quantitative measures of shape which the morphologists
have developed.)

Chapter six is on allometry --- the quantitative relations between different
parts or traits of the same organism (at one time or at different times), or
between the corresponding traits of different organisms. This is an old
subject, going back to D'Arcy Thompson
and even Galileo, but one which is still far from exhausted. Part of the
interest of the subject comes from the idea that allometric relations in
themselves explain some evolutionary changes: since metabolic rate goes up in
proportion to the three quarters power of body mass, then (so the argument
goes) if a lineage evolves to double its average body mass, it will
automatically evolve to increase its metabolic rate by a factor of 1.68 and
change. Harvey and Pagel are skeptical of this, and rightly so: very, very few
allometric relationships can be explained as simply a matter of physics. There
is usually some optimality criterion involved in their explanation, though
sometimes it's not made explicit. The three-quarters law for metabolism and
the many other quarter-power laws, for instance, seem to be consequence of minimizing the energy needed to
deliver nutrients and oxygen to the body's tissues by pumping fluids through
tubes. "[S]trong allometric trends may often indicate the presence of
strongly correlated selective pressures" (p. 177), so the comparative methods
developed earlier can be fairly directly applied to refining allometric
studies, which our authors proceed to do in some very nice worked examples.
(They also provide a good discussion of the different means of estimating
allometric parameters, but this does not depend on their comparative methods.)

There's been a lot of work on comparative
methods in the last eight years, but this book is still a fine introduction
to the modern, statistical-phylogenetic approach. Readers will need some
knowledge of both evolutionary theory and statistics (say an intermediate-level
course in both), but not expertise. The writing is clear throughout, with
technical asides being, in fact, set aside in boxes, and there are even hints
of a sense of humor (e.g., quoting the young Richard Lewontin on the
near-optimality of all animals). This book will be very useful to anyone
seriously studying evolution, and probably to others as well --- it's
easy to imagine adapting its methods to historical linguistics and other
studies of social change. The only objection to this book is its price, which
fails the xerox test by a factor of two.